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A preliminary disease survey in the wild Nile (Crocodylus niloticus) population in the ,

A J Lesliea*, C J Lovelya and J M Pittmanb

MATERIALS AND METHODS ABSTRACT The objective of this study was to conduct a preliminary survey of diseases that might be Study site present in the wild population in the Okavango Delta, Botswana. Botswana’s Okavango Delta, the samples were collected from ranging in size from 34.0 cm to 463.0 cm total length. world’s biggest Ramsar site (a of Samples were examined for blood parasites and underwent a haematological analysis. international importance), is a large wet- Before release the crocodiles were examined for various clinical abnormalities. Of the 144 land within the , covering crocodiles examined, none were visibly sick or displayed any signs of disease. No antibodies an area of approximately 16 000 km2 in to were detected. was present in 55.3 % of blood Mycoplasma crocodyli Hepatozoon pettiti the dry season and increasing to over smears examined, but there was no significant difference in any of the haematological 22 000 km2 with the annual flood. The values between the infected and uninfected crocodiles, and a high prevalence of Hepatozoon 2 infection is not uncommon in other . Only 7.6 % of the examined crocodiles were 111 250 km active catchment area falls infested with leeches. Further research is required for several of the crocodilian diseases, in entirely within . Owing to the particular to elucidate the role of wild crocodilians as reservoirs of infection. geology of the catchment, the incoming water is low in nutrients and sediment32. Keywords: Nile crocodile, Crocodylus niloticus, Okavango Delta, disease survey. The Okavango River flows through Leslie A J, Lovely C J, Pittman J M A preliminary disease survey in the wild Nile croco- briefly before entering Botswana dile (Crocodylus niloticus) population in the Okavango Delta, Botswana. Journal of the and forming a broad floodplain, the South African Veterinary Association (2011) 82(3): 155–159 (En.). Department of Conservation Panhandle. An estimated 40 % of incom- & Entomology, University of Stellenbosch, Private Bag X1, Matieland, 7600 South ing water leaks into the surrounding . swamps by the time the river leaves the Panhandle. The remaining 60 % is distrib- INTRODUCTION no other clinical signs and therefore uted down 3 main channels, which fan Since the development of the crocodile are not noticed to be unhealthy until out to form the Delta. The Okavango farming industry in the 1980s, a number they are found dead. Diseases causing Delta consists of permanent and seasonal of studies have been carried out world- visible external lesions, for example swamp, which is inundated during the wide on diseases in farmed croco- pox virus infection, are the obvious annual flood32. diles6,7,12,13,20,27,28. Very little, however, is exception. The northern part of the Delta is charac- known about the diseases of wild croco- (iv)Clinical examination has several limi- terised by shallow water, flooded grass- dilians, particularly wild Nile crocodiles. tations: cardiac and respiratory rates lands, ox-bow lakes and lagoons mostly Wild crocodiles are often difficult to study are variable according to conditions, interconnected by narrow waterways. owing to the remoteness of the areas in and are strongly influenced by capture Only a few main channels lined by tall which they occur. stress. Because crocodiles are poikilo- reeds (mainly Phragmites australis) carry The initial objective of this study was to thermic, body temperature cannot be the remainder of the Okavango’s water determine disease prevalence in the wild used as a diagnostic tool. southwards through the Delta. The per- Nile crocodile population in the Okavango (v) Sick/weak crocodiles are unlikely to manent and seasonal swamp together Delta. However, several factors made this survive for long due to . form a unique ecosystem and provide a difficult: Therefore, the likelihood of encoun- high-quality habitat for a great many (i) Very few serological tests have been tering these individuals in a capture species. As a keystone species, the Nile developed for crocodile diseases. and release survey is low. crocodile, helps maintain the fragile Consequently a serological survey is (vi)Owing to research permit limitations balance within this ecosystem. This of very limited value. no crocodiles could be sacrificed for includes selective predation on various (ii) Virus isolation is unavailable due to histopathological and parasitological fish species,10,42 recycling of nutrients and the lack of crocodile cell lines in veteri- examination. maintenance of wet refugia in times of nary diagnostic laboratories. In view of these limitations, it was pos- drought48. Crocodiles are unevenly dis- (iii)Sick crocodiles are difficult to identify tulated that a low incidence of diseases tributed throughout the Delta with the by observation. Under farmed condi- would be found in the Okavango popula- majority of the breeding population tions they often stop eating but show tion during a capture and release survey. occurring in the 120 km long Panhandle17. However, it was possible to do a more aDepartment of Conservation Ecology & Entomology, accurate survey for mycoplasmosis and Study University of Stellenbosch, Private Bag X1, Matieland, 7600 South Africa. haemogregarine infection thanks to the The Nile crocodile, Crocodylus niloticus, bJohannesburg Zoo, Private Bag X13, Parkview, 2122 availability of diagnostic tests. In addi- is the most widespread and abundant of South Africa. tion, ectoparasites, in the form of leeches, the 3 crocodile species that occur in Africa. *Author for correspondence. E-mail: [email protected] were easy to find, remove and count per It occurs throughout the continent south Received: July 2011. Accepted: August 2011. individual. of the Sahara in a variety of wetland habi-

0038-2809 Jl S.Afr.vet.Ass. (2011) 82(3): 155–159 155 tats, including coastal areas41,46. His- syringe was used, depending on the size into standard microhaematocrit tubes torically its distribution in southern Africa of the crocodile, and the blood was trans- and centrifuged for 5 min at 12 000 g. extended as far south as the Eastern Cape ferred directly into a lithium heparin tube. Total red cell counts (RCC) were per- Province during the past 100–200 years42. Blood smears were made from whole formed both manually and automatically Nile crocodiles are ectothermic and blood using the cover slip method24. Fol- using an electronic particle counter. The regulate their body temperature lowing blood collection, each crocodile automated counts were made using a behaviourally by moving between was measured (total length (TL) and Beckman Coulter Ac*T Series haematology sun-exposed sandbanks and the water. snout-to-vent length (SVL) using a flexible analyser (Coulter SA). The manual counts Typical adult lengths are around 3.5 m, measuring tape, ±1 mm). It was then were made using Natt and Herrick’s solu- but the males can grow up to 5 m18. Sexual weighed using a harness placed around tion. A 1:200 dilution was made by draw- maturity is reached from 2.9 m total the forelimbs and a Pesola spring balance. ing blood up to the 0.5 mark on a red length for males, and 2.2 m for females10. Each crocodile was sexed by cloacal exam- blood cell diluting pipette, then filling the Nesting occurs in a hole in the ground ination of the cliteropenis23,31 and the pipette to the 101 mark with Natt and and on average 50 eggs are laid. Nile croc- entire body was examined for clinical Herrick’s solution9. The diluted blood odiles exhibit temperature-dependent abnormalities including bite wounds, was then used to charge both counting sex determination31. Hatchlings emerge skin lesions, conjunctivitis, joint swelling chambers of an improved Neubauer after an incubation period of approximately and poor condition. Dorsal and lateral haemocytometer (Hawksley and Sons, 90 days in early to mid summer, and body surfaces were also examined for the Lancing, UK). After 5 mins in a humidity parental protection occurs39,40,41. As with presence of leeches. Leeches were removed chamber the red cells were counted in the other crocodilian species, a high mortality by means of a pair of tweezers, counted 4 corner cells and central cell of the central rate is experienced in their 1st year of life and stored in 70 % ethanol for later identi- large square of the counting chamber. due primarily to predation45. fication. This was repeated on the second chamber and the average multiplied by 10 000 to Capture methods Sample processing obtain the total red cell count per microlitre. One hundred and forty-four crocodiles On return to the field laboratory 1.0 m Haemoglobin concentrations (Hb) were were captured in the Panhandle of the of blood was transferred to an Eppendorf determined using a Beckman Coulter Okavango during summer (February tube for haematological analysis. The Ac*T Series haematology analyser (Coul- 2005). Capture was carried out using remaining blood was centrifuged using a ter SA). 2 methods. At night, using a 4.8 m manual desktop centrifuge and the Red blood cell indices were calculated flat-bottomed aluminium motor boat, plasma frozen for serology. If the volume using standard equations24 crocodiles were located with a spotlight of the blood sample was small it was allo- Mean cell volume: which revealed the eyes glowing red. The cated for either Hepatozoon examination MCV (fl) = PCV/RCC beam of light was then kept focused on or serology. the crocodile’s eyes, making it possible to Thirty-eight samples were examined for Mean cell haemoglobin: approach the animal by boat. Crocodiles blood parasites and underwent haemato- MCH (pg) = Hb (g/d ) × 10 / RCC estimated to be smaller than 1.2 m total logical analysis. Blood smears were Mean cell haemoglobin concentration: length were captured by hand. Croco- stained with Diff-Quick Stain (American 8 MCHC (g/d ) = Hb (g/d ) / PCV diles between 1.2 m and 2.3 m were Scientific Products, , USA) . The captured using a swivelling noose (Ani- presence of Hepatozoon gametocytes was Total white cell counts (WBC) were mal Handling Co., SA) which was placed determined by microscopic examination obtained indirectly using the Unopette over the snout and pulled tight in the of the Diff-Quick stained blood smears. A 5877 system (Becton-Dickinson, USA). neck region. Crocodiles were then minimum of 3 slides per animal and in The Unopette pipette was filled with brought onto the boat, jaws were taped some cases more were examined includ- blood (25 µ ) and mixed with the shut and the were physically ing a minimum of 1000 HPF’s (×100 oil phloxine B diluent in the reservoir. From restrained. Animals larger than 2.3 m immersion) per slide. The degree of this, both counting chambers of an were captured using a noose attached to a erythrocyte was estimated improved Neubauer haemocytometer climbing rope, which was secured to the by examining the red cell series and scor- were charged. After 5 min in a humidity boat. The crocodile was allowed to swim ing each slide on a scale of 1 to 4. chamber all the pink-staining granulo- so as to tire it out before it was brought On this scale, a score of 2 represented cytes were counted in both chambers. onto the boat. In addition to night capture, normal erythrocyte regeneration with Differential counts were done on the baited box and Pitman traps were strate- 10–20 % orthochromic erythroblasts but Diff-Quick stained smears. The percent- gically placed on river banks. Traps were no earlier stages. A score of 2.5 repre- age of heterophils and eosinophils was baited at sunset and checked at 1st light sented a moderate increase in erythrocyte calculated and used to calculate total the next morning. Captured animals were regeneration, with late polychromatic WBC9. immediately restrained, measured, exam- erythroblasts through to mature and Total WBC /µl = ined and samples collected. aging erythrocytes, while a score of 3 × ×× represented strong regeneration with Stained cells counted in chambers 1.1 16 100 Crocodile processing basophilic erythroblasts and early poly- Percentage heterophils and eosinophils Each crocodile was blindfolded and chromatic erythroblasts through to restrained in ventral recumbency. Fifty- mature and aging erythrocytes, but no The separated plasma was stored at three animals were randomly selected for proerythroblasts. Finally, a score of 4 –10 °C in a domestic gas freezer for up to blood collection. Blood was collected included all the other stages plus pro- 1 month. After return from the research from the post-occipital sinus9 on the dorsal erythroblasts. site, 30 samples were submitted to the midline and just caudal to the base of the Packed cell volumes (PCV) were deter- laboratory (Faculty of Veterinary Science, head. A 21 G (0.80 × 25–90 mm) or 23 G mined using a Statspin MP micro- Department of Veterinary Tropical Dis- (0.65 × 25 mm) needle and a 3, 5 or 10 m haematocrit centrifuge: blood was drawn eases, University of Pretoria) for serological

156 0038-2809 Tydskr.S.Afr.vet.Ver. (2011) 82(3): 155–159 testing for mycoplasmosis, using a plate Table 1: Size and haematological parameters of Hepatozoon-infected and uninfected agglutination test. crocodiles. Parameter Hepatozoon infected (n = 21) Hepatozoon negative (n = 17) Statistical analysis Haematological values were analysed Mean S.D. Mean S.D. for significant differences (P < 0.05) between Hepatozoon-infected and unin- SVL (cm) 46.3 22.4 38.2 12.3 Mass (kg) 3.80 6.39 1.74 2.65 fected crocodiles by 1-way analysis of PCV Haematocrit % 18.2 2.0 17.6 1.9 variance (ANOVA). The residuals were RCCRBC (×106/µ ) 0.62 0.14 0.56 0.08 checked for normality of distribution Hb (g/d ) 7.27 1.11 6.90 0.82 with normal probability plots. Where MCV (fl) 305.4 70.6 320.7 46.0 data were not normally distributed, MCH (pg) 121.5 31.8 125.2 13.7 significance was tested by means of a MCHC (g/d ) 39.7 2.7 39.4 3.9 Mann-Whitney test. Eryth. regener. index 2.4 0.4 2.3 0.4 WBCWCC (×103/µ ) 11.62 5.50 10.87 3.71 RESULTS Heterophils % 19.8 8.7 21.5 8.9 The crocodiles ranged in TL from Lymphocytes % 62.0 9.8 62.0 13.2 Monocytes % 1.0 2.2 0.6 1.1 34.0 cm to 46.3 cm, with a mean of 59.7 cm, Eosinophils % 6.0 5.1 3.5 4.1 and ranged in SVL from 25.5 cm to Basophils % 5.7 4.4 6.2 4.7 101.5 cm with a mean of 28.4 cm. Azurophils % 5.3 4.3 4.8 4.9 Of the 144 crocodiles caught and exam- Heterophils (×103/µ ) 2.00 0.62 2.19 0.89 ined, none were visibly sick or displayed Lymphocytes (×103/µ ) 7.43 4.10 6.93 3.49 any clinical signs of disease. The body Monocytes (×103/µ ) 0.11 0.22 0.07 0.11 condition of all the crocodiles was good. Eosinophils (×103/µ ) 0.65 0.58 0.38 0.51 3 The only external lesions observed were Basophils (×10 /µ ) 0.70 0.75 0.66 0.54 3 old healed bite injuries in one case, and a Azurophils (×10 /µ ) 0.70 0.91 0.48 0.46 recent puncture injury in another case. The only ectoparasite found on the Nile contrast, 6 of 17 (35.3 %) uninfected croco- plasmosis in crocodiles occurred in crocodiles examined was the leech diles displayed an increased rate of red Zimbabwe on 5 farms simultaneously34. Placobdelloides multistriatus. The leeches cell regeneration, with a mean score of 2.3 Rearing stock 1–3 years of age developed were identified with the aid of a key37,38. on the erythrocyte regeneration index. swollen limb joints and lameness. Eleven crocodiles were infested with the This was not a significant difference. Morbidity was 10 % and mortality even leech, a prevalence of 7.6 %. One croco- There was no significant difference lower. A new species of Mycoplasma was dile had 7 leeches, and another had 2. The between any of the haematological values cultured from the joints of affected remaining 9 parasitised crocodiles each of the infected and uninfected crocodiles animals and named Mycoplasma had a single leech. Leeches were found in (Table 1). The mean PCV and RCC of the crocodyli26. The disease was then repro- various places on the crocodiles, both infected group were 18.2 % and 0.62 × duced in healthy crocodiles by experi- dorsally and ventrally, for example on 106/µ , respectively, compared with 17.6 % mental infection with this isolate. the tail, neck, belly, armpits, between and 0.56 × 106 /µ in the uninfected group. Also in 1995 a highly fatal outbreak of webbing of back legs, and other sites. disease, characterised by arthritis and There was no obvious pattern of leech DISCUSSION pneumonia, occurred in farmed alligators distribution on the crocodiles. No correla- Owing to the limitations mentioned in (Alligator mississippiensis) in Florida2. Nine tion between current leech infestation the introduction it is probable that a out of 74 adult animals died over a 10-day and H. pettiti infection was found. capture and release survey does not period. A new species of Mycoplasma was No antibodies to Mycoplasma crocodyli provide a conclusive reflection of disease isolated and later named M. alligatoris3. were detected in any of the sera tested. prevalence in a crocodile population. On Losses continued over the next 6 months, Hepatozoon pettiti parasites were present the other hand, a very low disease inci- despite tetracycline treatment, until only in 21 of 38 blood smears examined dence in wild crocodiles is probable 14 alligators remained. An enzyme-linked (55.3 %). The mean SVL of the 38 croco- because stress is a very important predis- immunosorbent assay (ELISA) for the diles tested was 42.6 cm. The mean SVL of posing factor to disease in crocodiles. detection of antibodies produced by the infected crocodiles was 46.3 cm Crocodilians have been found to respond alligators in response to M. alligatoris ex- compared with 38.2 cm for the uninfected to non-specific stress with a chronic posure has since been developed4. crocodiles. The youngest infected croco- increase in corticosterone secretion, inhi- Following the initial outbreak in Zimba- dile in this study had a SVL of 25.5 cm. bition of growth, inhibition of the repro- bwe, cases of mycoplasmosis were re- Six of 8 females (75 %) and 13 of 27 males ductive system and suppression of the ported annually, from about 1/3 of (48 %) were infected. The sex of 2 croco- immune system30. Crocodiles living in a Zimbabwean crocodile farms. An auto- diles was undetermined due to their relatively pristine natural environment, genous vaccine was developed which, in small size. with a low population density, will not an experimental trial, afforded limited Two (9.5 %) of the infected crocodiles be exposed to the stress experienced by protection35. A subsequent severe out- were infested with leeches, as were 4 farmed crocodiles in an artificial, inten- break occurred in crocodiles following (23.5 %) of crocodiles negative for H. sive environment. Furthermore, trans- translocation, in which the morbidity was pettiti. mission of infectious diseases under over 50 % and the mortality rate over Of the 21 infected crocodiles, 10 (47.6 %) natural conditions is usually far slower 20 %33. Subsequently mycoplasmosis has showed an increased rate of red cell due to less –pathogen exposure become an important disease on South regeneration, with a mean score of 2.4 on compared with an intensive situation. African crocodile farms, with several the erythrocyte regeneration index. In The 1st recorded outbreak of myco- severe outbreaks having occurred (J

0038-2809 Jl S.Afr.vet.Ass. (2011) 82(3): 155–159 157 Picard, University of Pretoria, pers. schizonts are found in the liver of infected ans43. Leeches are a more common comm., 2006). crocodiles and gametocytes are found in crocodilian ectoparasite and have been The epidemiology of this disease is not erythrocytes or free in the blood. Sexual found on a few species including well understood. The source of the original multiplication occurs in the intermediate C. porosus52, Alligator mississippiensis14,15,25, Zimbabwean outbreak remains elusive. It host, usually haematophagous insects C. johnstoni51 and C. niloticus36,37. However, was suggested that wild crocodiles may and leeches25,29. little is known about the possible patho- act as reservoirs of infection, with vertical Hepatozoon pettiti was described in Nile genicity of the various species, although transmission being the main mode of crocodiles from Senegal and Uganda47 and leeches could possibly play a role in the transmission35. However, unidentified H. sheppardi was described from Nile croco- transmission of crocodile-specific viral mycoplasmas have been found in the diles in Mozambique44. Hoare19 was the and bacterial infections21 and as vectors of faeces of farmed Nile crocodiles, indicat- first to show transmission of H. pettiti by blood protozoans25. ing the possibility of horizontal transmis- the tsetse fly, Glossina palpalis. A later Placobdelloides multistriatus has been sion22. The concept of wild crocodilian study14 suggested that the leech P. multi- recorded as a parasite on crocodiles in reservoirs of infection has more recently lineata was a vector of haemogregarines Africa 10,36,37 although there is no previous been confirmed in the case of M. alligatoris. in alligators and this was supported by a record of its occurrence on crocodiles in In a seroprevalence study, 5.4 % of wild further study a few years later15. Fairly the Okavango region. A next step would American alligators were found to be recently it was confirmed that the species be to determine whether P.multistriatus is positive for M. alligatoris antibodies, at 12 found in crocodiles in the Okavango is a potential vector for H. pettiti infection in of 20 sites (60 %)5. Further elucidation of H. pettiti, although the vector is unknown the Okavango’s Nile crocodiles. the epidemiology of mycoplasmosis in at this stage16. Hepatozoon parasites are Further research is required on several Nile crocodiles requires that the status of thought to be apathogenic in their croco- of the crocodilian diseases to elucidate wild crocodiles be established. dilian hosts. In this survey, the aim was their epidemiology, and particularly the Many crocodile farms in southern to determine the prevalence of H. pettiti role of wild crocodilians as reservoirs of Africa (excluding South Africa) collect and its possible effect on the crocodile infection. Pox viruses, Adenovirus, West eggs from wild crocodile nests. If the wild host. Nile virus, chlamydiosis and mycoplas- population concerned is infected, this is a In a study which ran concurrently to mosis are all of particular interest. very risky practice. Often these farms are this one16, the authors found H. pettiti in obliged to reintroduce a certain number 61 out of 186 Nile crocodiles (32.8 %). As in ACKNOWLEDGEMENTS of juvenile individuals into the wild. If, on this study, no significant difference in the This research was supported by a the other hand, the wild population is PCV of infected and uninfected groups National Research Foundation and an free from mycoplasmosis, it could be was found. It is clear that there is a high Earthwatch Institute (USA) grant awarded disastrous to reintroduce infected juve- prevalence of H. pettiti infection in the to A J Leslie. The South African Veterinary niles. Okavango crocodile population, and that Foundation and the Johannesburg Zoo- At the time these samples were tested, it appears not to be pathogenic to the logical Gardens are acknowledged for the M. crocodyli plate agglutination test crocodile host. The mean SVL of the additional financial support. We thank had just been developed. It was believed Hepatozoon-infected crocodiles was greater Prof. Daan Nel (University of Stellen- that the test could identify recently in- than that of the uninfected group. It bosch) for helping with the statistical fected animals, but not old infections. would appear that crocodiles do not lose analysis and the Government of Botswana Subsequent testing on a positive farm the infection with increasing age. for providing the necessary research per- revealed that the test only identified very A very high prevalence of Hepatozoon in- mits. recent infection, as only animals that still fection is not uncommon in other species. had lesions tested positive (J Picard, Haemogregarina crocodilinorum was found REFERENCES pers. comm., 2006). The negative results to be widely distributed in the southern 1. Barnett J D, Cardeilhac P T,Barr B, Wolff W, obtained here do not, therefore, exclude United States and was found in 77 (59 %) Bass O L 1999 Differences between captive- 25 raised and wild-caught Everglades Na- historical infection with mycoplasms. 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